Phylogenomics, Spatiotemporal Transcriptional Dynamics and Cis-Regulatory Architecture Underlying the Portulaca oleracea Antioxidant Network Under Extreme Salinity.

Abstract

Global soil salinization severely threatens agricultural productivity. Portulaca oleracea L., an extreme xerohalophyte, displays exceptional salinity tolerance, yet the transcriptional architecture coordinating its antioxidant defenses across organs and developmental stages remains unresolved. In this study, multi-tissue high-throughput RNA-Seq, quantitative real-time PCR (qRT-PCR) validation, comparative phylogenomics across 154 plant genomes, and condition-specific gene regulatory network (GRN) modeling were integrated to characterize 436 antioxidant loci in P. oleracea. Under chronic hypersalinity (12 d), mature plants exhibited marked regulatory asymmetry: roots mounted a multi-tiered frontline defense driven by Fe/Mn-SOD (SOD2), cytosolic glutaredoxin 3 (50.24-fold induction), and class III peroxidases (PRX), whereas leaves suppressed multiple baseline peroxidase transcripts while selectively upregulating a putative secretory PRX (110.24-fold induction). Comparing developmental stages and stress durations revealed that juvenile leaves mounted a pronounced activation of glutathione-dependent pathways (GPX/GR) during acute osmotic stress, whereas adult foliage subjected to chronic salinity displayed a streamlined network consistent with catalase (CAT) post-transcriptional stabilization hypotheses and an upregulated glycine, serine, and threonine metabolic axis. GRN modeling predicted seven stress-specific candidate hub transcription factors (spanning the B3, LBD, C3H, AP2/ERF, and bHLH families), and promoter motif analysis identified a proximal GCC-rich element within salt-inducible CAT paralogs corresponding to putative AP2/ERF-binding sites. Together, these findings elucidate the organ-specific division of labor and cis-regulatory landscape underlying halotolerance in P. oleracea, providing prioritized candidate targets for engineering climate-resilient crops.